Permanent exclusive pairings are associated
with restructuring of themhc1system, where-
as the use of a consortial mating strategy is
associated with an almost complete loss of
bothmhc1andmhc2haplotype diversity. One
outlier in our analysis wasG. vanhoeffeni[TA];
this species exhibits a general reduction in
bothmhc1zandmhc2adiversity relative to
other temporarily attaching or nonattach-
ing species (table S4). The reason for this
reduction in MHC diversity in a tempora-
rily attaching species is unknown; however,
G. vanhoeffeni[TA]exhibits a number of addi-
tional immunological abnormalities, setting it
apart from other temporarily attaching species
(see below).
Pseudogenization of CD8 co-receptor genes
MHC class I–restricted CD8+cytotoxic T cells
are key mediators of allograft rejection ( 17 ).
Given that permanent attachment is associ-
ated with loss ofmhc1udiversity(tableS4),we
next examined thecd8aandcd8bgenes, which
encode the heterodimeric CD8abco-receptor
that interacts with MHC class I molecules ( 18 ).
Notably, functionalcd8aandcd8bgenes were
absent in all six permanently attaching spe-
cies; in two cases, remnants of thecd8agene
could be found in the interval between the
genes flanking the tandemly arrangedcd8a
andcd8bgenes (Fig. 2B and figs. S1 to S3).
Moreover, bothcd8genes were also missing
in the genome ofG. vanhoeffeni[TA], in line withthe lack of functionalmhc1ugenes in this spe-
cies (fig. S1 and table S4), further strengthening
its distinctive immunogenetic constellation
among the species with a temporary attachment
mode. Collectively, these findings suggest that
the canonical antigen-specific cytotoxic pathway
is impaired in all species distinguished by per-
manent male attachment. However, theperforin
gene (table S3), which encodes a key element of
the cytotoxic pathway, is present in all genomes
analyzed here, suggesting the presence of cy-
totoxic innate lymphoid cells in these species.Loss of the CD4 pathway
MHC class II–restricted CD4+helper T cells
are also known to play an important role in1610 25 SEPTEMBER 2020•VOL 369 ISSUE 6511 sciencemag.org SCIENCE
Fig. 2. Immunogenometic
features of lophiiform fishes.
(A) Number of shared and
distinctmhcgene alleles
in female-male pairs of the
two indicated species of
Ceratias. Blue indicates the
male genotype, and pink
indicates the female genotype.
(B) Tandem arrangement of
cd8bandcd8agenes and their
flanking geneszmat1andcast.
H. mollis[PAn]retains a short
sequence of the 5′end ofcd8a.
The structure of the locus
ofC. abei[NA]serves as a
reference; sequence homolo-
gies are indicated as shaded
blocks. (C) Gene models of
cd4-2andcd4-1. The relative
orientation of exons is
indicated by arrowheads.
Gray lines connect equivalent
exons between species. In
P. spiniceps[PAn], thecd4-2gene
has lost all exons except
exons 4 and 5, which are
found in an inverse orientation;
the first four exons ofcd4-1
are deleted, and remnants
of others exhibit deleterious
sequence alterations. Oblique
parallel black lines indicate
the omission of intergenic
sequence to highlight coding
features. (D) Gene model of
thecd3gdgene, which exhibits
deleterious changes inCeratias
species. Exons are depicted
as shaded blocks; internal
numbers indicate exon number,
whereas numbers flanking the
exons indicate the splice phase.
A 23–base pair deletion
(indicated by a black arrowhead) in exon 3 of theCeratiasgene causes a splicing defect, and mismatched splice sites are indicated with an asterisk. In addition,
theCeratias cd3gdgene exhibits the loss of the intron between exons 4 and 5.
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